From the Atlantic Forest of Serra De Paranapiacaba, Southestern Brazil
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ARTICLE The Muscidae (Diptera) from the Atlantic Forest of Serra de Paranapiacaba, southestern Brazil Silvio Shigueo Nihei¹³; Anderson Tatsuki Tamakoshi¹⁴; Priscylla Moll¹⁵ & Rodrigo Ferreira Krüger²⁶ ¹ Universidade de São Paulo (USP), Instituto de Biociências (IB‑USP), Departamento de Zoologia. São Paulo, SP, Brasil. ² Universidade Federal de Pelotas (UFPEL), Instituto de Biologia (IB), Departamento de Microbiologia e Parasitologia (DEMP). Pelotas, RS, Brasil. ³ ORCID: http://orcid.org/0000‑0002‑6887‑6282. E‑mail: [email protected] ⁴ ORCID: http://orcid.org/0000‑0003‑3954‑1018. E‑mail: [email protected] ⁵ ORCID: http://orcid.org/0000‑0002‑0226‑7732. E‑mail: [email protected] ⁶ ORCID: http://orcid.org/0000‑0003‑1040‑8299. E‑mail: [email protected] Abstract. A first survey of Muscidae in the State of São Paulo (Southeastern Brazil) is presented here with a one‑year of Malaise trap collecting from August 2010 to July 2011 at the Biological Reserve Alto da Serra de Paranapiacaba (23°46 00 ‑23°47 10 S, ′ ″ ′ ″ 46°18 20 ‑46°20 40 W, 750‑891 m of altitude). A total of 1,284 individuals of muscids were collected, and 15 genera and 39 ′ ″ ′ ″ species of Muscidae were identified. So far, only one muscid species had been recorded to the Reserve, which now has its Muscidae diversity increased to 40 species. Thirteen species are new records for the State of São Paulo. With this, the number of species of Muscidae species known to occur in the State of São Paulo is increased to 169. The interval between November and February was higher in number of individuals and number of species. Muscidae presented a seasonal pattern, with more abundance and diversity in that interval. The study area is covered by secondary forest and very close to São Paulo metropolitan area, and the composition of the fauna of Muscidae signalizes this environment changing and anthropic stress with nine species with synanthropic habits, two of them are typically synanthropic species. Keywords. Diversity; Inventory; Neotropical region; Seasonality; State of São Paulo; Survey. INTRODUCTION the different Brazilian biomes and states. For ex- ample, while there is a voluminous literature on The family Muscidae is worldwide distribut- Muscidae for the States of Paraná and Rio de ed and include about 5,200 described species in Janeiro (e.g., Carvalho et al., 1984; D’Almeida, 187 genera (Pape et al., 2011). In the Neotropical 1991; Pamplona et al., 2000; Oliveira et al., 2002; Region there are over 800 species and 85 gen- Costacurta et al., 2003; Couri & Carvalho, 2005; era (Couri & Carvalho, 2005). The family is greatly Leandro & D’Almeida, 2005; Rodríguez-Fernández abundant in all continents, occurring in most oce- et al., 2006; Couri & Barros, 2009), the most rich anic islands, and also in the Arctic and regions of and populous Brazilian State remains with the tundra vegetation (Huckett & Vockeroth, 1987). Muscidae diversity knowledge still incipient. Muscid flies have diverse feeding habits, includ- Furthermore, it is relatively scarce the Muscidae ing predators, phytophagous, saprophagous, surveys in the Neotropics based on the use of anthophilous, parasites and haematophagous non-baited collecting techniques (e.g., Carvalho (Couri, 1999; Savage & Vockeroth, 2010; Carvalho & Couri, 1991; Costacurta et al., 2003; Rodríguez- et al., 2012). Fernández et al., 2006; Krüger et al., 2010; Zafalon- There are a number of studies with invento- Silva et al., 2018). The present study is the first ex- ry of Diptera in the Neotropics (e.g., Carvalho & haustive survey of Muscidae for the State of São Couri, 1991; Couri et al., 2000; Pamplona et al., Paulo based on non-baited collectings. Previous 2000; Krüger et al., 2010; Borkent et al., 2018; surveys focused on urban and/or cadaveric fauna Zafalon-Silva et al., 2018), on the other hand, sev- (Linhares, 1981; Dias et al., 2014; Cavallari et al., eral studies focused on groups with agricultural 2015). In Brazil, 358 species are described and or forensic importance (e.g., Ferraz et al., 2009; recorded, 156 of these occur in the State of São Mulieri et al., 2011; Garcia et al., 2003; Cavallari Paulo (Lowenberg-Neto & Carvalho, 2013, with et al., 2015; Carvalho et al., 2017; Olea et al., 2017). updates from Pereira-Colavite & Carvalho, 2012; With regard to Muscidae, there are a number of Cavallari et al., 2015; Fogaça & Carvalho, 2018). inventories in Brazil, but unbalanced between In this article we surveyed the Muscidae of the Pap. Avulsos Zool., 2021; v.61: e20216168 ISSN On-Line: 1807-0205 http://doi.org/10.11606/1807-0205/2021.61.68 ISSN Printed: 0031-1049 http://www.revistas.usp.br/paz ISNI: 0000-0004-0384-1825 http://www.scielo.br/paz Edited by: Carlos José Einicker Lamas Received: 07/05/2021 Accepted: 26/05/2021 Published: 30/07/2021 Pap. Avulsos Zool., 2021; v.61: e20216168 Nihei, S.S. et al.: Muscidae from Paranapiacaba 2/12 Biological Reserve Alto da Serra de Paranapiacaba (State MATERIAL AND METHODS of São Paulo, southeastern Brazil) in the Atlantic Forest biome, and analyzed its abundance, diversity and sea- Study area and collection sonality throughout a one-year collecting period. So far, only one muscid species had been recorded to the This survey took place in the Biological Reserve Alto Biological Reserve of Paranapiacaba (Townsend, 1927; da Serra de Paranapiacaba (Fig. 1) (23°46 00 , 23°47 10 S; ′ ″ ′ ″ Lowenberg-Neto & Carvalho, 2013). 46°18 20 , 46°20 40 W, 750-891 m of altitude), located ′ ″ ′ ″ Figure 1. Location of the Biological Reserve Alto da Serra de Paranapiacaba, State of São Paulo, southeastern Brazil (23°46 00 , 23°47 10 S; 46°18 20 , 46°20 40 W, ′ ″ ′ ″ ′ ″ ′ ″ 750‑891 m of altitude). Nihei, S.S. et al.: Muscidae from Paranapiacaba Pap. Avulsos Zool., 2021; v.61: e20216168 3/12 in the municipality of Santo André, State of São Paulo, tervals (95%) as a function of abundance was performed Brazil. The reserve is situated slightly under the Capricorn in R using the statistical package iNEXT (Hsieh et al., Tropic (23°27 S), in a transition area between the Tropical 2016) based on the methodologies proposed by Colwell ′ and the Subtropical climates zones (Gutjahr & Tavares, et al. (2012) and Chao et al. (2014). 2009). According to Köppen’s classification, the climate Collector curves were obtained for the Biological type is Cwa, temperate and humid, with dry winter Reserve Alto da Serra de Paranapiacaba and for each sea- and hot summer. The mean temperature at summer sonal season within the same area. (December-March) is 20 , and 14 on winter (June- ℃ ℃ September), with temperature range of 6 (Gutjahr & ℃ Tavares, 2009). The area is predominantly covered with RESULTS secondary Atlantic Forest under different successional stages, and that altered flora is due to historical anthrop- Within the one-year of Malaise trap collected ma- ic intervention (Sugiyama et al., 2009), as this area is very terial, seven families of Calyptrata were surveyed: close to São Paulo metropolitan area. Calliphoridae, Fanniidae, Mesembrinellidae, Muscidae, Insects were collected using Malaise traps, installed Rhinophoridae, Sarcophagidae and Tachinidae. Those at three different point of the Reserve: trap 1 was locat- seven families accounted a total of 3,451 individuals, ed at 23°46 38 S, 46°18 42,7 W; trap 2 at 23°46 44.6 S, with Muscidae as the most abundant, with 1,284 indi- ′ ″ ′ ″ ′ ″ 46°18 40,2 W; and trap 3 at 23°46 45,7 S, 46°18 29,2 W. viduals (37%). Excluding the genera formerly belonging ′ ″ ′ ″ ′ ″ Traps were installed and material had been collected to “Coenosiinae” (sensu Carvalho et al., 2005), the collect- continuously from August 2010 to July 2011. Sampling ed material of Muscidae was restricted to 397 individu- vessels were replaced monthly, and the collected materi- als, and a total of 15 genera and 39 species of Muscidae al taken to the lab for sorting and identification. were identified (Table 1 and Appendix) from the three subfamilies of Muscidae: Muscinae, Cyrtoneurininae and Mydaeinae (following the subfamilial classification sensu Identification Haseyama et al., 2015). Thirteen species are new records for the State of São Paulo: Dolichophaonia machadoi The specimens were recognized until the genera and (Albuquerque, 1958), D. simplex (Albuquerque, 1958), species level, using identification keys in Carvalho (2002). Helina discreta (Wulp, 1896), H. gigantea Albuquerque, When necessary, taxonomic revisions were consulted, 1956, H. regobarrosi Albuquerque, 1958, Neomuscina containing updated identification keys and descriptions anajeensis Pereira-Colavite & Carvalho, 2012, N. trans- (e.g., Pereira-Colavite & Carvalho, 2012; Nihei & Carvalho, porta Snyder, 1949, Neurotrixa sulina Costacurta & 2007; among others). All studied material was pinned Carvalho, 2005, Phaonia advena Snyder, 1957, P. annu- and, in most cases, males and/or females were dissect- lata (Albuquerque, 1957), P. grandis (Couri, 1982), P. len- ed to study their terminalia, which were compared to tiginosa Snyder, 1957 and Polietina minor (Albuquerque, drawings and descriptions in the literature. The dissect- 1956). With this, the number of species of Muscidae ed terminalia were cleared with 10% KOH solution, then known to occur in the State of São Paulo is increased to neutralized with acetic acid solution and washed with 169. water; after examination, they were stored in microvials Quantitative data analysis reveals that the interval with glycerine and pinned with the respective specimen. between November and February had both more indi- The material was deposited at the Museu de Zoologia, viduals (Fig. 2) and more species (Fig. 3) collected. Those Universidade de São Paulo, São Paulo (MZSP). three-month period have a sequence of 60-55-56 indi- viduals, while other months reached up to 36 individuals. For species number, we had a variation of 14 to 18 spe- Data analyses cies. Shannon diversity index confirms summer with the highest diversity, followed by spring, autumn and winter Quantitative data were analyzed by calculating (Table 2).